Nesbitt - Differences in Soil Quality Indicators Between Organic and Sustainably Managed Potato Fields in Canada

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    Ecological Indicators 37 (2014) 119130

    Contents lists available at ScienceDirect

    Ecological Indicators

    journal homepage: www.elsevier .com/ locate /ecol ind

    Differences in soil quality indicators between organic and sustainably

    managed potato fields in Eastern Canada

    Johanna E. Nesbitt a, Sina M. Adl a,b,

    a Department of Biology, Dalhousie University, Halifax, NS,Canada, B3H4J1b Department of Soil Science, University of Saskatchewan, Saskatoon, SK,Canada, S7N5A8

    a r t i c l e i n f o

    Article history:

    Received 2 April 2013Received in revised form 13 August 2013

    Accepted 1 October 2013

    Keywords:

    Agro-ecosystem

    Bio-indicators

    Farming systems

    Organic agriculture

    Soil ecology

    Soil quality

    a b s t r a c t

    The aim ofthis study was to determine iforganic management offields promoted soil quality indicators

    compared to sustainably managed fields following best-management practice guidelines. Using a soil

    quality minimum data set, conventionally and organically managed commercial potato fields in eastern

    Canada were compared. Microbial biomass, testate amoebae, nematodes, and microarthropods served as

    bioindicators, while soil pH, C:N ratio, light fraction, bulk density, and soil moisture served as the chemical

    and physical indicators. We also investigated whether differences in site location (different soil texture

    and local climate) were more or less important than field management (organic or conventional). When

    site location and seasonal factors were considered, the soil quality indicators were better at differentiating

    organic and conventional potato fields. There was no single indicator that could clearly differentiate, on

    its own, between the two field managements due to variability with site location or month ofsampling.

    Microbial biomass, testate amoebae, microarthropod and soil moisture varied significantly through the

    growing season. The mean soil pH, C:N ratio, and moisture were significantly different between sites.

    However, the indicators were affected to different degrees, and differed to some extent to both site

    location and time ofsampling. The results ofthis study also provide a baseline for similar soil quality

    evaluations in management of eastern Canada potato fields. We recommend that several indicators,

    including bioindicators should be used together, and that several sites should be sampled. In addition,

    one-time field sampling ofan indicator, as it has been often practiced by growers, is likely to give falseresults as it does not account for variability through the growing season.

    2013 Elsevier Ltd. All rights reserved.

    1. Introduction

    Intensification of agriculture was accompanied with increased

    use of synthetic fertilizers, pesticidesand herbicides that has raised

    concerns regarding their side-effect on the environment. In reac-

    tion to this, a variety of sustainable agriculture practices have

    gainedpopularity,as well as organic agriculture as an alternative to

    the intensive inputs in conventional agriculture. These sustainable

    practices include adding organic matter to the soil, covering soil

    with cover crops or crop residues,reducingtillage intensityor prac-

    ticing conservation tillage, using legumes within a crop rotation,

    implementing strip cropping, improving drainage, and avoiding

    compaction (Madgoff, 2001; Kennedy and Papendick, 1995). Best

    management practices were proposed to reduce the amount of

    synthetic chemicals used in conventional agriculture while main-

    taining acceptable levels of economic return (Hilliard and Reedyk,

    Corresponding author at: Department of Soil Science, University of

    Saskatchewan,Saskatoon, SK, Canada, S7N 5A8. Tel.: +1 306966 6866.

    E-mail address: [email protected](S.M. Adl).

    2000; Korol, 2004). Organic agriculture claims to be environmen-

    tally sustainable, socially just, and economically sound production

    practices but prohibits using most synthetic fertilizers, herbicides,

    and pesticides, as well as other restrictions (Lotter, 2003; El-Hage

    Scialabba and Hattam, 2002; Biao et al., 2003). Increasing soil

    biological activity in order to maintain long term soil fertility

    through decomposition of the organic matter are the first priori-

    ties of organic agricultural management practices (IFOAM, 2011;

    Fliessbach and Mader, 2000; Biao et al., 2003). In this study we

    compared conventional fields under best management practise to

    fields under organic agriculture.

    Soil quality is a key element in evaluating the sustainability of

    agriculture practices (Carter, 2002). By combining Brookes (1993)

    criteria, Doran and Parkins (1994) criteria, and Doran and Safleys

    (1997) criteria, Stenberg (1999) produced a list of five essential

    criteria used in determining proper soil quality indicators. Because

    soil functions are difficult to measure, soil properties that are sen-

    sitive to change in a specific ecosystem are often used as indicators

    of soil quality (Stenberg, 1999; Acton and Padbury, 1993). A min-

    imum data set is a group of soil quality indicators that are chosen

    based on a definition of soil quality and soil quality indicator

    1470-160X/$ see front matter 2013 Elsevier Ltd. All rights reserved.

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    120 J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130

    criteria (Larson and Pierce, 1991; Doran and Parkin, 1994; Harris

    et al., 1996). Modern studies have argued that physical, chemi-

    cal, and biological indicators must be evaluated together in order

    to provide a correct assessment of soil quality (Stenberg, 1999;

    Wander and Bollero, 1999; Stenberg et al., 1998; Gomez et al.,

    2004; Schloter et al., 2003a). However, a comprehensive analysis

    of soil will not accurately describe soil quality unless the indi-

    cators are chosen with a specific soil function in mind, within a

    defined ecosystem (Janzen et al., 1992; Stenberg, 1999; Acton and

    Padbury, 1993). In this study, we focused on potato production

    within the eastern Canada Maritimes and indicators were selected

    accordingly.

    Potatoes (Solanum tuberosum L.) are the third most important

    food crop in the world and play an important role in feeding the

    worlds population (International Potato Center, 2011). Potato pro-

    ductionineasternCanadacontinuestoincreaseandproducesabout

    1,772,000 tonnes annually, and it is the main crop from this region

    (Agriculture Canada, 2011). However, potato nutrient demand on

    soil is high, andtuberquality requires both high organic matter and

    nitrogen availability. The intense use of synthetic chemicals, as fer-

    tilizer and pathogen control, in conventional potato production has

    also caused concern for the adjacent waterways and the surround-

    ing environment (Patriquin et al., 1991). Sustained conventional

    potato monoculture as practised is leading to decreased outputper

    hectare without substantially increasingchemical inputs, thus rais-

    ing costs (Saini andGrant, 1980; Porter andMcBurnie, 1996; Carter

    et al., 1998, 2003). To sustain soil fertility and production levels,

    more sustainable forms of potato production have been proposed

    (i.e.rotations and spring tillage) thatwould reduce production costs

    (Porter and McBurnie, 1996; Patriquin et al., 1991; Carter et al.,

    1998).

    In this study we tested the hypothesis that fields under each

    management practice (conventional-best management or organic-

    management) would not be different based on indicators of soil

    quality. The two management practices were chosen because they

    are claimed to be sustainable. Potato fields were chosen because

    of the significance of this food crop in the region and globally.

    Although other soil quality studies have been conducted on potatofields in Prince Edward Island (Canada) and Maine (U.S.A.) (Carter,

    2002; Porter and McBurnie, 1996; Carter et al., 2003), this is the

    first study to include bioindicators and to compare fields across the

    region. It is also the first study to compare two types of sustainable

    practices in potato production in the region.

    2. Materials and methods

    2.1. Soil sampling

    Three conventional and three organic potatofields were chosen

    within a 150 km radius for a total of six field sites. All six sites werecommercial farms, not experimental fields. Each organic field was

    located within a few kilometres of a conventional field. Fields were

    sampled in each of May, July, andSeptember withinone day of each

    other. For each field, soil samples were collected at three locations

    on a randomly selected diagonal transect across the field. Samples

    were taken inthe middleof thepotatohill,approximately1520 cm

    from the stem, to a depth of 10 c m. At each sampling location,

    separate samples were collected for nematode, testate amoebae,

    soil pH, C:N ratio, and soil moisture using a 2.5cm soil corer, as

    described below. Similarly, separate samples for microarthropod,

    light fraction and bulk density were taken using a 5 cm soil corer,

    and microbial biomass was measured from a 1kg composite soil

    sample. Soil samples were transported to the lab in a cooler where

    they were processed within 24h of sampling.

    2.2. Field sites

    The first organic management field (O1) is an easilydrained fine

    sandy loam Charlottetown series soil, but has a small percentage

    of easily drained fine sandy loam Alberry soil as well. The farm has

    been under cultivation since the mid 1900s, but was converted to

    organic agriculture over a seven year period (19932000) and was

    certified in 2000. Parasol 50% (copper hydroxide, fungicide) was

    applied twice, Bluestone (copper sulphate, fungicide) was applied

    twice, and Entrust (spinosad, insecticide) was applied once during

    the 2004 growing season. Potato tops were physically cut off at the

    end of the season.

    The first conventional management field (C1) is an easily

    drained fine sandy loam of the Charlottetown series. The land has

    been under potato cultivation since 1942. The potato rows were

    seededalongside a bandfertilizer of NPK-Mg. Lorox (linuron, herbi-

    cide)was applied once,Manzate(mancozeb, fungicide)was applied

    six times, Ridol-Bravo was applied once, Bravo (chlorothalonil,

    fungicide) was applied three times, and mineral oil was applied

    five times throughout the 2004 growing season. Reglone (diquat

    dibromide (37.3%), desiccant/herbicide) was applied twice at the

    end of the season as a top kill.

    The second organic management field (O2) is a poorly draining

    clay loam Washburn series soil. The farm has been in cultivationsince 1980 and was certified organic in 1987. The rotation used in

    this field is manure, clover, potatoes, and then mixed vegetables.

    Parasol wasapplied three times andEntrust wasapplied twice dur-

    ing the 2004 growing season. A propane flamer wasused atthe end

    of theseason tocleanup late blight, as a final ColoradoPotato Beetle

    control and as a top-kill.

    The second conventional management field (C2) is on a poorly

    drained silty loam of the Interval series. The land has been under

    cultivation since the early 1800s. The rotation includes corn, bras-

    sica, and potatoes. Chemical applications to the field did occur but

    were not recorded.

    Thethirdorganicmanagementfield(O3) is found onlightbrown

    sandy loam of the Torbrook series with good to excessive drainage.

    The farm has been under organic cultivation since 1988. The rota-tion consists of potatoes, two years of mixed vegetables, followed

    by a green manure of oats and peas which are left in through the

    winter and harrowed under in the spring. Floating row covers are

    used to speed the early stages of growth, and to avoid pests and

    disease.

    Thethirdconventional management field (C3) is found on sandy

    loam Truro series soil with good to fair drainage. Admire (imidac-

    loprid, insecticide) and an NPK fertilizer were banded in furrow

    when the crop was seeded. An N fertilizer was also broadcast

    on the crop mid-growing season. Sencor (herbicide) was applied

    once, Bravo was applied three times, and Tatoo C (fungicide) and

    Cymbush (cypermethrin, insecticide/miticide) were applied once

    throughout the growing season. Reglone was applied once as a top

    kill.

    2.3. Soil quality indicator measurements

    Microbial biomass C was measured using chloroform

    fumigation-extraction according to standard procedures (Paul

    et al. , 1999). On each sampling occasion, a composite sample of

    approximately 1 kg of soil was taken from each field. The soil

    was sieved using a 2.83cm diameter sieve and organic particles

    larger than 3 m m were removed by hand. The fumigated and

    unfumigated extracted filtrates were stored in 50mLfalcon tubes

    at 20 C until the chloroform labile C analysis was analysed with

    a LECO CNS auto-analyser.

    Testate amoebae were stained and enumerated using standard

    procedures (Adl et al., 2006a) from three 2.5 cm10cm deep soil

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    J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130 121

    cores taken at each sampling site of every field (3 samples per

    field). One soil composite was obtained from each sampling site

    and three subsamples of 1g placed into each of three test tubes.

    This resulted in three 1 g subsamples per soil sample for a total of

    nine test tubes per field. The slides were dried on a slide dryer and

    examined under one drop of glycerine with a cover slide. Three

    4cm long transects were observed at 400 on a Zeiss compound

    microscope. The number of stained testate amoebae were enumer-

    ated along each transect to obtain abundances from line transects

    (Krebs, 1998).

    Nematodes were extracted and enumerated according

    to standard procedures (Coleman et al., 1999) from three

    2.5cm10 c m soil cores per sampling location (3 sampling

    sites per field) and combined into one composite soil core for

    each sampling site. Three subsamples of known weight (48g)

    were extracted per sampling location and stored in 5% formalin.

    Nematodes were enumerated with a Nikon inverted microscope

    at 100 and functional groups were identified at 400.

    Microarthropods were extracted and enumerated according to

    standard procedure (Coleman et al., 1999). Two 5cm10cm deep

    soil cores were taken per field sampling site (3 samples per field),

    weighed and placed into an extraction cup. The microarthropods

    were collectedin 95% ethanol andenumerated in a Petri dish with a

    Nikon dissectingmicroscope. The samples were enumerated at 30

    andidentified at 80 to sub-order(mites) or to family (collembola).

    Soil pH, light fraction (LF), bulk density (BD) and gravimet-

    ric water content were obtained according to Robertson et al.

    (1999). The soil C:N ratio was measured according to Elliott et al.

    (1999) fromsix compositefield samples that were airdried, ground

    to

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    May July September

    -1000

    0

    1000

    2000

    3000

    4000

    Micro

    arthropodAbundance

    g-1drysoil

    0

    2000

    4000

    6000

    Tes

    tateAmoebae

    g-1drysoil

    0

    20000

    40000

    60000

    80000

    100000

    Field and Month

    ChloroformLabileC

    ugg-1drysoil

    0

    100

    200

    300

    400

    500

    May

    July

    September

    Nem

    atodeAbundance

    g-1drysoil

    0

    10

    20

    30

    50

    100

    150

    200

    250

    300

    350

    20000

    30000

    40000

    50000

    60000

    70000

    Organic

    Conventional

    Month

    0

    5

    10

    15

    20

    25

    O1 C1 O2 C2 O3 C3

    A B

    C D

    E F

    G H

    Fig. 1. Bioindicators measuredin organically managed fields(O1, O2,O3) and in conventional fields (C1,C2, C3).Pooled dataof all organic (filled circle) or conventional(clear

    circle) fields foreach month.

    biomass, as implied from chloroform labile carbon, increased over

    the growing season in every field (Fig. 1a). Fields under organic

    management had the highest chloroform labile C means in the

    soil, throughout the growing season, compared to conventional

    fields (Fig. 1b). Mean testate amoebae and nematode abundance

    was more variable between field sites through the growing season

    (Fig. 1c and d). When combining all organic and all conventional

    field sites, mean abundance for both decreased over the growing

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    Table 2

    Nematode functional groupabundance means (with standard error)with respect to theinteraction effects of therandomized block designgeneral linearmodel.

    Nematodes(g1) Bacterivores Fungivores Root feeders Omnivores Predators

    Management practice

    Organic 12 (3) 0 (0) 2 (1) 0 (0) 0 (0)

    Conventional 5 (2) 0 (0) 3 (1) 0 (0) 0 (0)

    Month

    May 10 (3) 0(0) 1 (1) 0 (0) 0 (0)

    July 9 (3) 0 (0) 4 (1) 0 (0) 0 (0)

    September 6 (3) 2 (1) 2 (1) 0 (0) 0 (0)

    Management practicemonth

    Organic

    May 17 (4) 0 (0) 1 (2) 0 (0) 0 (0)

    July 12 (4) 1 (0.2) 2 (2) 0 (0) 0 (0)

    September 8 (5) 0 (0) 2 (2) 0 (0) 0 (0)

    Conventional

    May 4 (4) 0 (0) 2 (2) 0 (0) 0 (0)

    July 6 (4) 0 (0) 5 (2) 0 (0) 0 (0)

    September 4 (4) 1 (0.3) 3 (2) 0 (0) 0 (0)

    Location

    A 7 (3) 0 (0) 4 (1) 0 (0) 0 (0)

    B 8 (3) 0 (0) 1 (1) 0 (0) 0 (0)

    C 11 (3) 1 (0.2) 2 (1) 0 (0) 0 (0)

    Means were estimated with Fishers least significant difference withP= 0.05, type III sum of squares.

    season (Fig. 1e and f). There was no significant difference in tes-

    tateamoebae mean abundances between organic and conventional

    fields (Fig. 1d). Mean nematode abundance in the organic fields

    was higher than in conventional fields in every month sampled,

    but this was not statistically significant. Among the nematode

    functional groups, bacterivore, fungivore, root feeder, predator,

    and omnivore. Means and standard errors were analysed by ran-

    domized block design (Table 2). Nematode functional groups did

    not significantly differ between organic and conventional fields,

    samplingdate, the interaction between managementand datesam-

    pled, or between locations (Tables 2 and 3). Mean microarthropod

    abundance was higher in September in most field sites sampled

    except in C3 (Fig. 1g), and this was significantly higher for organic

    fields (Fig. 1h, Tables 1 and 4). Mean abundance of mite subor-

    ders and Collembola families did not significantly differ between

    organic and conventional fields, months sampled, interaction

    between management practice and month, or between locations

    (Table 5).

    3.2. Physical and chemical indicators

    When organic fields were combined, soil pH was fairly stable

    over the growing season, but in the conventional fields the mean

    soil pH decreased slightly through the growing season (Fig. 2a and

    b, Table 1). The mean C:N ratio was consistently higher in the con-

    ventional fields than in the organic fields, but increased over the

    growing season in the organic fields (Fig. 2c and d). Light fraction

    was measured at the beginning and at the end of the growing sea-

    son, in May and September. Mean light fraction weight remained

    significantly higher in the organic fields compared to conventional

    Table 3

    Effect of management practice, month sampled, their interaction, and location on nematode functional groups.

    Effect Statistic Value F Error d.f. p-Value Significance

    Management practice

    Pillais trace 0.754 3.05 5 0.123 NS

    Wilks lambda 0.25 3.05 5 0.123 NS

    Hotellings trace 3.05 3.05 5 0.123 NS

    Roys largest root 3.05 3.05 5 0.123 NS

    Month

    Pillais trace 1.201 1.78 12 0.170 NS

    Wilks lambda 0.06 2.97 10 0.050 *

    Hotellings trace 10.69 4.28 8 0.025 NS

    Roys largest root 10.30 12.36 6 0.004 **

    Management practicemonth

    Pillais trace 1.192 1.75 12 0.1777 NS

    Wilks lambda 0.09 2.42 10 0.089 NS

    Hotellings trace 7.53 3.01 8 0.066 NS

    Roys largest root 7.08 8.49 6 0.011 *

    Location

    Pillais trace 0.903 0.99 12 0.498 NS

    Wilks lambda 0.26 0.97 10 0.518 NS

    Hotellings trace 2.26 0.90 8 0.569 NS

    Roys largest root 1.93 2.32 6 0.168 NS

    Abbreviations and symbols:d.f. (degreesof freedom), typeIII sumof squares wereused, NS (notsignificant), ***p0.001, 1, 2, 3, 4orderof theeffectscontributionto the overall

    model.* p0.05.

    **

    p0.01.

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    124 J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130

    Field and Month

    0.000

    0.001

    0.002

    0.003

    0.004

    0

    2

    4

    6

    8

    0

    2

    4

    6

    8

    10

    12

    14

    16

    May

    July

    September

    0.0

    0.2

    0.4

    0.6

    0.8

    1.0

    1.2

    1.4

    SoilpH

    5.0

    5.2

    5.4

    5.6

    5.8

    6.0

    6.2

    6.4

    C:N

    Ratio

    7

    8

    9

    10

    11

    12

    Organic

    Conventional

    Month

    May July September

    BulkDensity

    gcm-3

    0.8

    0.9

    1.0

    1.1

    LightFraction

    g-1drysoil

    0.0000

    0.0005

    0.0010

    0.0015

    0.0020

    0.0025

    A B

    C D

    E F

    G H

    O1 C1 O2 C2 O3 C3

    Fig.2. Physicaland chemicalindicatorsin organicallymanagedfields(O1,O2, O3)and in conventionalfields(C1,C2, C3).Pooleddataof allorganic(filledcircle)or conventional

    (clear circle) fields foreach month.

    fields, with a slight butnot-significant difference, over the growing

    season (Fig. 2e and f). Over the growing season, mean bulk density

    decreased from May to July to September in all fields except C2

    (Fig. 2g). Conventional sites had a consistently higher mean bulk

    density than theorganic fields (Fig.2h). Soil moisture at each samp-

    ling time showed the organic fields retained significantly higher

    mean soil moisture content than the conventional fields at the time

    of sampling (Table 1).

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    Table 5

    Effect of management practice, month sampled, their interaction, and location on mite and collembolan abundances.

    Effect Value F Error d.f.a p-Valueb

    Management practice

    Pillais trace 0.983 5.27 1 0.327 NS

    Wilks lambda 0.02 5.27 1 0.327 NS

    Hotellings trace 47.42 5.27 1 0.327 NS

    Roys largest root 47.42 5.27 1 NS

    Month 0.572

    Pillais trace 1.632 0.99 4 0.361 NS

    Wilks lambda 0.00 2.18 2 NS

    Hotellings trace 154.22 0.00 0 0.029 NS

    Roys largest root 152.45 33.88 2 NS

    Management practicemonth

    Pillais trace 1.711 1.32 4 0.433 NS

    Wilks lambda 0.00 1.65 2 0.443 NS

    Hotellings trace 70.67 0.00 0 NS

    Roys largest root 68.02 15.11 2 0.064

    Location

    Pillais trace 0.284 18.00 4 0.975 NS

    Wilks lambda 0.21 18.00 2 0.979 NS

    Hotellings trace 0.00 18.00 0 NS

    Roys largest root 1.10 9.00 2 0.562 NS

    NS, not-significant;1,2,3,4 order of effects contribution to theoverall model;type IIIsum of squares.a

    Degrees of freedom.b Significance.

    Table 6

    Meansand standard errorsof the soil quality indicators with respect to management practice, month, and location,usingthe randomized block generalized linearmodel.

    Indicators Microbial biomass

    (mg g1)

    Testate amoebae

    (# g1)

    Nematodes

    (# g1)

    Micro-arthropods

    (# g1)

    Soil pH C:N ratio Bulk density

    (gcm3)

    Soil moisture

    (%)

    Management practice

    Organic 242.64 (13.2) 50,100 (5200) 15 (3) 1450 (250) 6.06 (0.1) 9.99 (0.5) 0.905 (0.02) 22.38 (0.8)

    Conventional 136.12 (14.7) 47,305 (4700) 9 (3) 660 (230) 5.53 (0.1) 11.46 (0.4) 1.107 (0.01) 15.89 (0.7)

    Month

    May 135.74 (14.7)a 66,000 (5800) a 12 (4) a 300 (280) a 5.93 (0.1) a 10.17 (0.5) a 1.096 (0.02) a 19.57 (0.9) a

    July 202.63 (14.7)b 45,000 (5800)ab 13 (4) a 354 (280) a 5.74 (0.1) a 10.76 (0.5) a 1.066 (0.01) a 16.77 (0.9) b

    September 229.77 (16.8) b 35,100 (6600) b 9 (4) a 2510 (320) b 5.72 (0.1) a 11.26 (0.6) a 1.160 (0.02) a 21.07 (1.0) ab

    Location

    A 171.40 (14.7) a 48,900 (5800) a 11 (4) a 1020 (280) a 5.16 (0.1) a 10.19 (0.5) a 0.984 (0.03) a 15.70 (0.9) a

    B 202.00 (14.7) a 44,200 (5800) a 10 (4) a 1200 (280) a 6.40 (0.1) b 12.83 (0.5) b 1.022 (0.03) a 21.52 (0.9) b

    C 194.74 (16.8) a 53,000 (6600) a 14 (4) a 950 (320) a 5.82 (0.1) a 9.16 (0.6) a 1.042 (0.05) a 20.19 (1.0) ab

    Means estimated using Fishers least significant difference with p= 0.05. Values within the same column labelled with the same letter are not significantly different from

    each other, according to Tukeys honestly significant difference calculated atp= 0.05.

    Fig. 3. Canonicalcorrespondence analysisbiplot of soil quality indicators, manage-

    ment practices and month sampled.

    Fig. 4. Canonical correspondence analysis biplot of management practices and

    month sampled.

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    J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130 127

    Table 7

    Effect of management practice,monthsampled, their interaction,and location on soil quality,with respect to theinteractioneffects of therandomized block designgeneral

    linear model.

    Effect Statistic Value F Error d.f. p-Value Significance

    Management practice

    Pillais trace 0.994 21.01 2 0.046 *

    Wilks lambda 0.01 21.01 2 0.046 *

    Hotellings trace 84.04 21.01 2 0.046 *

    Roys largest root 84.04 21.01 2 0.046 *

    Month

    Pillais trace 1.961 20.64 6 0.01 **

    Wilks lambda 0.00 15.28 4 0.009 **

    Hotellings trace 135.66 8.48 2 0.110 NS

    Roys largest root 97.49 36.56 3 0.007 **

    Management practicemonth

    Pillais trace 1.893 6.44 6 0.015 *

    Wilks lambda 0.00 5.33 4 0.059 NS

    Hotellings trace 52.78 3.30 2 0.257 NS

    Roys largest root 42.29 15.86 3 0.022 *

    Location

    Pillais trace 1.922 8.93 6 0.006 **

    Wilks lambda 0.00 6.45 4 0.042 *

    Hotellings trace 55.86 3.49 2 0.245 NS

    Roys largest root 38.85 14.57 3 0.025 *

    Abbreviations and symbols: d.f. (degrees of freedom), type IIIsum of squares were used, NS (not significant),1,2,3,4

    order of theeffects contribution to theoverall model.* p0.05.** p0.01.

    Table 8

    Effect of management practice, month sampled, their interaction,and location on thesoil quality indicatorlight fraction.

    Effect Light fraction (g LF g1 dry soil) F d.f. p-Value Significance

    Management practice

    Organic 0.00182 (0.0003) 5.77 1 0.061 NS

    Conventional 0.00080 (0.0003)

    Month

    May 0.00137 (0.0003) 0.09 1 0.776 NS

    September 0.00124 (0.0003)

    Management practicemonth

    Organic May 0.00194 (0.0004) 0.08 1 0.787 NS

    September 0.00169 (0.0005)

    Conventional May 0.00080 (0.0004)

    September 0.00079 (0.0004)

    Location

    A 0.00246 (0.0003) 7.83 2 0.029 *

    B 0.00087 (0.0003)

    C 0.0060 (0.004)

    Abbreviations and symbols: d.f. (degrees of freedom), type IIIsum of squares were used, NS (not significant).* p0.05.

    the smaller the deviation from the grand mean of all the envi-

    ronmental variables (Jongman et al., 1995). When the organic and

    conventional fields, and May, July and September scores were sep-

    arated, the organic, conventional, andJuly scores were shown to be

    multicolinear (Table 9 and Fig. 3). When organic and conventionalvariables were combined into a single variable called management

    practice, and May, July, and September were combined into a sin-

    gle variable called month in CCA biplot B, all multicolinearity was

    eliminated(Table9 and Fig.4). The eigenvalues, percentages, cumu-

    lative percentages and speciesenvironment correlations of both

    biplots are shown in Table 9. Both CCA biplots illustrate the same

    correlations and relationships between variables.

    Theoccurrenceof testate amoebae close to thecentre of theplotindicates they were not sufficiently affected by management prac-

    tise or by any of the other variables to be useful indicators in this

    study. The microarthropods indicate they are strongly responsive

    Table 9

    Canonical correspondence analysis of soil quality indicators, filed site management practices and month sampled.

    CCA Biplot, Fig. 3 CCA Biplot, Fig. 4

    Axis one Axis two Axis one Axis two

    Eigenvalues 0.044 0 0.035 0

    Percentage 52.715 0.398 41.833 0.212

    Cumulative percentage 52.715 53.113 41.833 42.045

    Indicator-environment correlations 0.732 0.505 0.654 0.329

    Multicollinearity detected Organic, conventional, July

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    128 J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130

    Table 10

    Intraset correlations between environmental variables and constrained site scores ofFigs. 3 and 4.

    CCA Fig.3 CCA Fig. 4

    Scores Envi. axis 1 Envi. axis 2 Scores Envi. axis 1 Envi. axis 2

    Organic 0.076 0.379 Mngt pract 0.011 0.242

    Conventional 0.076 0.379

    May 0.436 0.725 Month 0.887 0.231

    July 0.226 0.825

    September 0.792 0.057

    % moisture 0.229 0.193 % moisture 0.155 0.569

    Bulk density 0.581 0.159 Bulk density 0.583 0.320

    pH 0.195 0.194 pH 0.134 0.502

    C:N ratio 0.379 0.263 C:N ratio 0.212 0.305

    to the local climate, season and month of sampling, as well as soil

    pH, moisture and C:N ratio, but negatively affected by higher bulk

    density. The seasonal effect dominates their abundance dynamics

    and they are therefore not useful to distinguish between the two

    management practices in this study. The microbial biomass esti-

    mated from chloroform labile C also responded in the same way as

    the microarthropods, but to a lesser extent, and higher biomass

    correlated more strongly with organic management. The nema-

    todeabundancewas strongly affected by managementpractiseandhigher abundance correlated more with organic management. The

    light fraction weightwas higherin organic plots (Table 6 and Fig.2).

    The environmental indicators alsorespondedto month of sampling,

    showing higher moisture, pH and C:N ratio towards September,

    but lower bulk density in September in part caused by potato

    tuber mounding. Overall the organic fields correlated with higher

    pH, moisture, nematode abundance, micro-arthropod abundance,

    microbial biomass, and lower bulk density and C:N ratio. The con-

    ventional fields under best management practise correlated with

    higher bulk density, higher C:N ratio, lower pH, and lower abun-

    dance of bioindicators.

    4. Discussion

    4.1. Soil management effect on soil quality indicators

    Soil quality indicators were meant to be practicaland fast meas-

    ures to determine health or fertility levels of soils. When chosen

    well, indicators can be used to monitor field sites and to make

    management decisions. One needs to exercise caution as there are

    studies that exerted huge effortonlyto conclude thewrongbioindi-

    cator was selected (Geissen and Kampichler, 2004). The indicators

    selected for this study were chosen because they had been pro-

    posed as useful indicators in the literature. However, as this study

    shows,not allindicatorsare usefulfor thesamepurpose. Some indi-

    catorswere betterused forcertain comparisons, butnot others. For

    example, some indicators may discriminate between large differ-ences between sites (such as a forest and an agriculture field), but

    not smaller differences between similar fields under agriculture. In

    addition, the level of taxonomic resolution used in bio-indicators

    may be more significant than abundance measures typically used.

    Furthermore, our results show that, predictably, indicators fluc-

    tuate with month of sampling through the growing season and

    with site location. Therefore, for soil quality indicators a one-time

    measurement does not suffice, reducing the practicality of such

    measures. Using an aggregate of indicators, with sufficient samp-

    ling through the growing season, as well as multivariate statistical

    analysis of the data provide better indicators of field management

    effects on soil. Our results show that our minimum data set of

    indicators, when used together, could differentiate between

    organic and conventional best-practice potato fields.

    When used on their own, the indicators provided mixed results,

    some showing no significant difference while others detecting

    differences (Table 1): individually, six of the nine soil quality indi-

    cators included in the minimum data set differed between organic

    and conventional fields. Some indicators responded more to site

    location or month than fieldmanagement. For nematode functional

    groups, mite suborders, or collembolan family, the abundances

    were not significantly different, using a variety of statistical meas-

    ures (Tables 25). However, we note not all statistical techniqueswere consistent, so that comparing several is useful. Better dis-

    crimination between organic and conventional best-practice fields

    was obtained when the fields were averaged by management

    (Tables 6 and 7). The indicators detected significant overall differ-

    ences between organic and best-practice management, and were

    less affected by month of sampling or site location. The multivari-

    ate CCA results provided a better visualization of correspondences

    among the indicators (Table 10 and Figs. 3 and 4).

    4.2. Interactions among indicators andwith management

    Overall, the general linear model and the canonical correspon-

    dence analysis showed fields under organic management had

    higherpH,soilmoisture,litterlightfraction,andlowerC:Nratioandbulk density than the conventional fields. Given the emphasis on

    the role of the soil food web in decomposition and mineralization

    in organic agriculture, it was expected that organic management

    would promote soil conditions that were favourable for biological

    activity (Neher, 1999a,b; Fliessbach and Mader, 2000). However,

    conventional fields under best management practice were not sig-

    nificantly different from the organic fields for testate amoebae

    and nematode abundances. The organic fields supported higher

    microarthropod abundance but the significant microarthropod

    effect is due to the elevated abundance in the organic fields in

    September. Only microbial biomass was significantly higher in the

    organic fields, and this was probably affected by the lower bulk

    density and lower C:N ratio in these fields. The organic field mean

    C:N ratio (= 9 .99) and the conventional field mean C:N ratio(= 1 1.46) were below 20:1 (Table 6), which may indicate the

    predominance of the bacterial energy channel (Ferris and Matute,

    2003). Dendooven et al. (2000) also reported significant differ-

    ence between their low conventional and organic soil C:N values

    (CON= 8 and ORG= 5). Their study suggests that the low C:N ratio

    could be attributed to differences in C availability, to differences in

    microbialbiomassC:N ratios, todifferencesin N dynamics,or todif-

    ferences that cannot be reflected in the measurements of organic

    and conventional practices (Dendooven et al., 2000). Lower bulk

    density suggests that the soil in the organic fields was favourable

    to biological activity (Harris et al., 1996). When used as a physical

    soil quality indicator in comparisons of organic and conventional

    soil bulk density, results in other studies have differed. In a field

    experiment by Bulluck et al. (2002) organic and synthetic fertility

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    J.E. Nesbitt, S.M. Adl / Ecological Indicators37 (2014) 119130 129

    amendments were compared. The organic fertilizer, comprised of

    cotton-gin trash, compostedyard waste and cattle manure showed

    a decrease in bulk density, while the synthetic fertilizer did not

    (Bulluck et al., 2002). In a study of three groups of organic and

    conventional fields, organic field bulk density was shown to be

    significantly higher in the first group, not significantly different in

    the second group, and significantly lower in the third group com-

    pared to the conventional counterpart (Schjnning et al., 2002).

    Schjnning et al. (2002) suggest that their results indicate that

    soil compaction due to extensive traffic may reach the same lev-

    els in organic fields as is currently experienced in conventional

    fields.

    Higher microbial biomass and microarthropod abundance in

    organic fields may indicate a difference in the quality (C:N ratio)

    or availability of plant litter and compost amendments, since both

    are strongly related to resource quality and availability (Wardle

    and Lavelle, 1997; Wardle et al., 1999). The lower soil C:N ratio

    (higher quality)in organic fieldswould support an increased micro-

    bial biomass, however microarthropods generally thrive on lower

    quality organic matter (higher C:N ratio) (Wardle and Lavelle, 1997;

    Georgieva et al., 2005). Microarthropod abundance is known to be

    heavily influenced by resource quality andavailability, buthas also

    varied with management practice (Behan-Pelletier, 1999, 2003;

    Mebes and Filser, 1998; Wardle et al., 1999). In other comparisons

    of organic and conventional fields, as in this study, both testate

    amoebae and nematode abundances have been shown not to dif-

    fer significantly (Foissner, 1997; Neher, 1999b). Testate amoebae

    abundance has been cited as a poor indicator of agriculture man-

    agement practices differences, while nematode abundances were

    expected to differentiate between differing managementpractices,

    months and provinces (Georgieva et al., 2005). Our study agrees

    with the literature, that the majority of the nematodes found in

    organic soils are bacteriovores, and the remaining population is

    made upof rootfeeders (Neher, 1999b). Bacteriovores (both nema-

    todes and protozoa) have been suggested as better indicators of

    bacterial activity, substrate quality, and nutrient release in the

    soil than direct measurement of bacterial populations (Georgieva

    et al., 2005). If decomposition and nutrient mineralization hadbeen more efficient in the organic systems, indicated by higher

    microbial biomass and microarthropod abundance, the abundance

    of bacterivorous nematodes and testate amoebae should have

    been significantly higher as well. Neher (1999b) suggests that the

    nematode communities in organic and conventional fields are too

    similar, supporting the view that even with the lack of inorganic

    inputs, the organic soil food web composition is not as different

    from a conventional soil food web as was once thought. Although

    testate amoebae, nematode, and microarthropod abundance are

    standard bioindicators that have traditionally been enumerated

    (Behan-Pelletier, 1999; Foissner, 1999; Neher, 2001), species rich-

    ness and diversity may be more useful indicators of soil quality

    and soil health (Naeem, 2002; Adl et al., 2006b). However, it is

    most likely that the fields under best-management practice arenot all that different biologically from fields near-by under organic

    management.

    After discussions with the growers, it became evident that the

    organic fields were managed with more frequent tillage than the

    fields under best-management practice. We therefore sought a no-

    tillage potato field under organic management in the area. We

    compared our data to the same quality indicators in the no-till

    organic potatoplot forthe monthof September. Theresults suggest

    thatwithouttillage,the plots underorganicmanagement haveboth

    more functional diversity and higher abundance of indicator orga-

    nisms, and are significantly different from the best-management

    practice fields (Nesbitt, unpublished). This is consistent with previ-

    ous observations on the effect of tillage on soil diversity (Adl et al.,

    2006b).

    5. Conclusion

    Using a combination of indicators that included physical, chem-

    ical and biological parameters provided a better evaluation of the

    field sites, than if a single or fewer indicators are selected. Indica-

    tors varied through the growing season so that multiple sampling

    times are necessary to infer any conclusions on field manage-

    ment. Bioindicators under best-management-practice were not

    that different from the organic management fields. We suggest the

    increased tillage frequency in the organic fields is responsible for

    preventing a recovery of the biodiversityand organism abundance.

    The differences in physical parameters between both management

    practices are most likely due to the increased organic matter in the

    fields under organic practice. This increased abundance of some

    bioindicators but not to the point of being consistently significant.

    Acknowledgements

    This research was supported by a NSERC grant to S.M.A. We

    thank the Dalhousie University Faculty of Graduate Studies, the

    School for Resource and Environmental Studies, and the Soil Ecol-

    ogySocietyfor their financialsupport andtravel awardsto J.E.N.We

    thank the potato growers that co-operated with this study, pro-vided access to fields and information about field management:

    Raymond Loo, Lori Robinson, Karen Davidge, Gordon Harvey, Nor-

    bert Kungl, Kris Pruski.

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